Adaptive responses of miniature rose to cultivation modes and abiotic stresses

Abstract

Key message

The miniature rose-bush architecture may be improved by abiotic stresses applied to plants grown under short cultivation mode, which results in their enhanced robustness, branching and blooming capacity.

Abstract

Miniature rose-bushes of the Meikanrou variety, grown in the annual cycle and submitted to vegetative break during winter (“long” cultivation mode, LCM), developed more solid and branched frame with multiple blooms than those grown in an accelerated 4-month cycle, under constant conditions of light and temperature (“short” cultivation mode, SCM). Plants grown under both cultivation modes displayed significant differences in sugars and amino acids content, pH variations of the vascular sap, as well as modified ATPase proton pumping activity. The main biological question to address was whether abiotic stresses (chemical, mechanical and water), applied under SCM conditions might improve horticultural quality by mimicking those of the LCM plants. Notable cyto-histological modifications were observed in stem vascular tissues of the fourth internode under each of the three abiotic stresses. The chemical stress led to increased syringyl/guaiacyl ratio, and thereby, to cell wall strengthening. The mechanical stress displayed the most pronounced decrease of stem length/diameter ratio, favoring the frame robustness. The most pertinent result concerned the controlled water depletion, which not only appeared able to override the reduced branching under SCM conditions, but also further enhanced it to a level similar to that in plants grown under LCM. The application of the chemical, mechanical and water stresses differentially improved branching, stem fortification and blooming capacity of rose-bushes grown under the SCM conditions, thereby providing promising horticultural applications.

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References

  1. Amborabé BE, Bonmort J, Fleurat-Lessard P, Roblin G (2008) Early events induced by chitosan in plant cells. J Exp Bot 59:2317–2324

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  2. Albersheim P, An J, Freshour G, Fuller MS, Guillem R, Ham KS, Hahn MG, Huang J, O’Neil M, Whitcombe A, Williams MV, York WS, Darwill A (1994) Structure and function studies of plant cell wall polysaccharides. Biochem Soc Trans 22:374–378

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  3. Alvez G, Ameglio T, Guilliot A, Fleurat-Lessard P, Lacointe A, Sakr S, Petel G, Julien JL (2004) Winter variation in xylem sap pH of walnut trees: involvement of plasma membrane H+-ATPase of vessel associated cells. Tree Physiol 24:99–105

    Article  Google Scholar 

  4. Atanassova R, Favet N, Martz F, Chabbert B, Tollier M-T, Monties B, Fritig B, Legrand M (1995) Altered lignin composition in transgenic tobacco expressing O-methyltransferase sequences in sense and antisense orientation. Plant J 8:465–477

    CAS  Article  Google Scholar 

  5. Babin V (1995) Transport des nutriments dans le tissu xylémien de Populus x euramericana 1214. Thèse Univ Poitiers, Etude à l’échelle tisulaire et membranaire

    Google Scholar 

  6. Balla J, Kalousek P, Reinohl V, Friml J, Prochazka S (2011) Competitive canalization of PIN-dependent auxin flow from axillary buds controls pea bud outgrowth. Plant J 65:571–577

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  7. Barbier F, Péron T, Lecerf M, Perez-Garcia MD, Barriere Q, Rolcik L (2015) Sucrose is an early modulator of the key hormonal mechanisms controlling bud outgrowth in Rosa hybrida. J Exp Bot 66:2569–2582

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  8. Barnola P, Lavarenne S, Gendraud M, Jallut N (1986) Etude biochimique d’une dormance rythmique chez le frêne (Fraxinus excelsior) cultivé en conditions contrôlées. CR Acad Sci Paris 303:239–244

    CAS  Google Scholar 

  9. Bennett T, Sieberer T, Willett B, Booker J, Luschnig C, Leyser O (2006) The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr Biol 16:553–563

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  10. Besombes S, Mazeau K (2005) The cellulose/lignin assembly assessed by molecular modeling. Part 2: seeking for evidence of organization of lignin molecules at the interface with cellulose. Plant Physiol Biochem 43:277–286

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  11. Blakeney AB, Harris PJ, Henry RJ, Stone BA (1983) A simple and rapid preparation of alditol acetates for monosaccharide analysis. Carbohyd Res 113:291–299

    CAS  Article  Google Scholar 

  12. Boyer N, Gaspar T, Lamond M (1979) Modifications des isoperoxydases et de l’allongement des entre noeuds de la Bryone à la suite d’irritations mécaniques. Z Pflanzenphysiol 93:459–470

    Google Scholar 

  13. Boyer N, Desbiez MO, Hofinger M, Gaspar T (1983) Effect of lithium on thigmomorphogenesis in Bryonia dioica. Ethylene production and sensitivity. Plant Physiol 72:522–525

    Google Scholar 

  14. Boyer N, De Jaegher G, Bon MC, Gaspar T (1986) Cobalt inhibition of thigmomorphogenesis in Bryonia dioica: possible role and mechanism of ethylene production. Physiol Plant 67:552–556

    CAS  Article  Google Scholar 

  15. Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  16. Chabbert B, Monties B, Zieslin N, Ben-Zaken R (1993) Lignin content and composition of rose flower peduncles differing by their resistance to bending. Plant Physiol Biochem 31:241–247

    CAS  Google Scholar 

  17. Choubane D, Rabot A, Mortreau E, Legourrierec J, Peron T, Foucher F, Ahcène Y, Pelleschi-Travier S, Leduc N, Hamama L, Sakr S (2012) Photocontrol of bud burst involves gibberellin biosynthesis in Rosa sp. J Plant Physiol 169:1271–1280

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  18. Choudhury S, Panda S, Sahoo L (2013) Reactive oxygen species signaling in plants under abiotic stress. Plant Signal Behav 8(4):e23631

    Article  CAS  Google Scholar 

  19. Demotes-Mainard S, Huché-Thélier L, Morel P, Boumaza R, Guérin V, Sakr S (2013) Temporary water restriction or light intensity limitation promotes branching in rosebush. Sci Hortic 150:432–440

    Article  Google Scholar 

  20. Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, Ehrismann JS, Jurgens G, Estelle M (2005) Plant development is regulated by a family of auxin receptor F box proteins. Dev Cell 9:109–119

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  21. De Jaegher G, Boyer N, Gaspar T (1985) Thigmomorphogenesis in Bryonia dioica: changes in soluble and wall peroxidases, phenylalanine amonia-lyase activity, cellulose, lignin content and monomeric constituents. Plant Growth Regul 3:133–148

    Article  Google Scholar 

  22. De Jaegher G, Boyer N (1987) Specific inhibition of lignification in Bryonia dioica. Effects on thigmomorphogenesis. Plant Physiol 84:10–11

    PubMed  PubMed Central  Article  Google Scholar 

  23. Emamverdian A, Ding Y, Mokhberdoran F, Xie Y (2015) Heavy metal stress and some mechanisms of plant defense response. Sci World J 2015:756120. https://doi.org/10.1155/2015/756120

    Article  Google Scholar 

  24. Essiamah SK (1980) Spring sap of trees. Plant Biol 93:257–267. https://doi.org/10.1111/j.14388677.1980.tb03337.x

    CAS  Article  Google Scholar 

  25. Ferguson AR, Eiseman JA, Leonard JA (1983) Xylem sap from Actinidia sinensis: seasonal changes in composition. Ann Bot 51:823–833

    Article  Google Scholar 

  26. Ferguson BJ, Beveridge CA (2009) Roles for auxin, cytokinin and strigolactone in regulating shoot branching. Plant Physiol 149(4):1929–1944

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  27. Fromard L, Babin V, Fleurat-Lessard P, Fromont JC, Serrano R, Bonnemain JL (1995) Control of vascular sap pH to the vessel associated cells in woody species. Plant Physiol 108:913–918

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  28. Geilfus CM (2017) The pH of the apoplast dynamic factors with functional impact under stress. Mol Plant 10:1371–1386

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  29. Girault T, Bergougnoux V, Combes D, Viemont JD, Leduc N (2008) Light controls shoot meristem organogenic activity and leaf primordia growth during bud burst in Rosa sp. Plant Cell Environ 31:1534–1544

    PubMed  Article  PubMed Central  Google Scholar 

  30. Girault T, Abidi F, Sigogne M, Pelleschi-Travier S, Boumaza R, Sakr S, Leduc N (2010) Sugars are under ligth control during bud burst in Rosa sp. Plant Cell Environ 33:1339–1350

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Hernández-Hernández V, Rueda D, Caballero L, Alvarez-Buylla ER, Benítez M (2014) Mechanical forces as information: an integrated approach to plant and animal development. Front Plant Sci 5:265. https://doi.org/10.3389/fpls.2014.00265

    Article  PubMed  PubMed Central  Google Scholar 

  32. Hosokawa M, Suzuki S, Umezawa T, Sato Y (2001) Progress of lignification mediated by intercellular transportation of monolignols during tracheary element differentiation of isolated Zinnia mesophyll cells. Plant Cell Physiol 42:959–968

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  33. Hsiao TC (1973) Plant responses to water stress. Annu Rev Plant Physiol 24:519–570

    CAS  Article  Google Scholar 

  34. Iiyama K, Wallis AFA (1990) Determination of lignin in herbaceous plants by an improved acetyl bromide procedure. J Sci Food Agric 51:145–161

    CAS  Article  Google Scholar 

  35. Jaffe MJ, Forbes S (1993) Thigmomorphogenesis: the effect of mechanical perturbation on plants. Plant Growth Regul 12(3):313–324

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  36. Jaffe MJ, Huberman M, Johnson J, Telewski FW (1985) Thigmomorphogenesis: the induction of callose formation and ethylene evolution by mechanical perturbations in bean stems. Physiol Plant 64:271–279

    CAS  Article  Google Scholar 

  37. Jia WS, Davis WJ (2007) Modification of leaf apoplastic pH in relation to stomatal sensitivity to root-sourced abscisic acid signals. Plant Physiol 143:68–77

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  38. Karuppanapandian T, Geilfus CM, Mühling KH, Novák O, Gloser V (2017) Early changes of the pH of the apoplast are different in leaves, stem and roots of Vicia faba L. under declining water availability. Plant Sci 255:51–58. https://doi.org/10.1016/j.plantsci.2016.11.010

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. Kehrer JP (2000) The Haber-Weiss reaction and mechanisms of toxicity. Toxicology 149:43–50

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  40. Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  41. Kieber JJ, Schaller GE (2018) Cytokinin signaling in plant development. Development 145:dev149344. https://doi.org/10.1242/dev.149344

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. Kramer PJ, Boyer JS (1995) Water relations of plants and soils. Academic Press, San Diego, London

    Google Scholar 

  43. Lachaud S, Catesson AM, Bonnemain JL (1999) Structure and functions of the vascular cambium. C R Acad Sci Paris 322:633–650

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  44. Lapierre C (1993) Application of new methods for the investigation of lignin structure. In: Jung HG, Buxton DR, Hatfield RD, Ralph J (eds) Forage cell wall structure and digestibility. American Society of Agronomy, Crop Science Society of America, Soil Science Society of America, Madison, USA, pp 133–165

    Google Scholar 

  45. Leduc N, Roman H, Francois B, Thomas P, Huché-Thelier L, Lothier J (2014) Light signaling in bud out growth and branching in plants. Plants 3:223–250. https://doi.org/10.3390/plants3020223

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  46. Le Gall H, Philippe F, Domon JM, Gillet F, Pelloux J, Rayon C (2015) Cell wall metabolism in response to abiotic stress. Plants 4:112–166

    PubMed  PubMed Central  Article  Google Scholar 

  47. Leroux O (2012) Collenchyma: a versatile mechanical tissue with dynamic cell walls. Ann Bot 110:1083–1098

    PubMed  PubMed Central  Article  Google Scholar 

  48. Li-Marchetti C, Le Bras C, Relion D, Citerne S, Huché-Thélier L, Sakr S, Morel P, Crespel L (2015) Genotypic differences in architectural and physiological responses to water restriction in rose-bush. Front Plant Sci 6:1–14

    Article  Google Scholar 

  49. Marafon AC, Herter FG, Hawerroth FJ, Neutzling Bierhals A (2016) Free amino acids in the xylem sap of pear trees during dormancy. Ciênc Rural 46:1136–1141. https://doi.org/10.1590/0103-8478cr20131515

    Article  Google Scholar 

  50. Meents MJ, Watanabe Y, Samuels AL (2018) The cell biology of secondary cell wall biosynthesis. Ann Bot 121:1107–1125. https://doi.org/10.1093/aob/mcy005

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  51. Mothes K, Engelbrecht L (1961) Kinetin-induced directed transport of substances in excised leaves in the dark. Phytochemistry 1:58–62

    CAS  Article  Google Scholar 

  52. Mothes K, Engelbrecht L, Schütte HR (1961) Über die Akkumulation von α-Aminoisobuttersäure im Blattgewebe unter dem Einfluss von Kinetin. Physiol Plant 14:72–75

    CAS  Article  Google Scholar 

  53. Noronha H, Silva A, Dai Z, Gallusci P, Rombolà AD, Delrot S, Gerós H (2018) A molecular perspective on starch metabolism in woody tissues. Planta 248:559–568. https://doi.org/10.1007/s00425-018-2954-2

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  54. Noubhani M, Sakc S, Denis MH, Delrot S (1996) Transcriptional and post transcriptional control of plant plasma membrane H+-ATPase by mechanical treatments. Biochem Biophys Acta 1281:213–219

    PubMed  Article  PubMed Central  Google Scholar 

  55. Pesquet E, Zhang B, Gorzsás A, Puhakainen T, Serk H, Escamez S, Barbier O, Gerber L, Courtois-Moreau C, Alatalo E, Paulin L, Kangasjärvi J, Sundberg B, Goffner D, Tuominen H (2013) Non-cell-autonomous postmortem lignification of tracheary elements in Zinnia elegans. Plant Cell 25:1314–1328. https://doi.org/10.1105/tpc.113.110593

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  56. Pezet-Si MY (1987) Caracterisation des potentialités morphogènes de Castanea sativa Miller. Distribution et possibilité de translocation des réserves insolubles et solubles associées à des gradients de pH intracellulaire. Thèse Univ. Clermont-Ferrand

  57. Rabot A, Henry C, Ben Baaziz K, Mortreau E, Azri W, Lothier J (2012) Insight into the role of sugars in bud burst under light in the rose. Plant Cell Physiol 53:1068–1082

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  58. Reichmann SM (2002) The response of plant to metal toxicity: a review focusing on copper, manganese and zinc. Australian Minerals and Energy Environment Foundation, Melbourne, Australia. ISBN 1-876205-13-X

  59. Riou-Khamlichi C, Menges M, Healy JM, Murray JA (2000) Sugar control of the plant cell cycle: differential regulation of Arabidopsis D-type cyclin gene expression. Mol Cell Biol 20:4513–4521

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  60. Santoni V, Vansuyt G, Rossignol M (1991) The changing sensitivity to auxin of the plasma membrane H+-ATPase: relationship between plant development and ATPase content in membranes. Planta 185:227–232

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  61. Sauter JJ (1988) Seasonal changes in the efflux of sugars from parenchyma cells into the apoplast in poplar stems (Populus X canadensis”robusta”). Trees 7:242–249

    Google Scholar 

  62. Sauter JJ, Ambrosius T (1986) Changes in the partitioning of carbohydrates in the wood during bud break in Betula pendula Roth. J Plant Physiol 124:31–43

    CAS  Article  Google Scholar 

  63. Sauter JJ, Van Cleve B (1992) Storage, mobilization and interrelations of starch, sugar, protein and fat, in ray storage tissue of poplar trees. Trees 8:297–304

    Article  Google Scholar 

  64. Schneider A, Godin C, Boudon F, Demotes-Mainard S, Sakr S, Bertheloot J (2019) Light regulation of axillary bud outgrowth along plant axes: an overview of the roles of sugars and hormones. Front Plant Sci 10:1–17. https://doi.org/10.3389/fpls.2019.01296

    Article  Google Scholar 

  65. Shao HB, Chu LY, Jaleel CA, Zhao CX (2008) Water-deficit stress-induced anatomical changes in higher plants. CR Biol 331:215–225

    Article  Google Scholar 

  66. Subramanian S, Cho UH, Keyes C, Yu O (2009) Distinct changes in soybean xylem sap proteome in response to pathogenic and symbiotic microbe interactions. BMC Plant Biol 9:119. https://doi.org/10.1186/1471-2229-9-119

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  67. Suzuki K, Baba K, Itoh T, Sone Y (1998) Localization of xyloglucan in cell walls in a suspension culture of tobacco by rapid-freezing and deep-etching techniques coupled with immunogold labelling. Plant Cell Physiol 39:1003–1009

    CAS  Article  Google Scholar 

  68. Szabados L, Savouré A (2009) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  69. Tenhaken R (2015) Cell wall remodelling under abiotic stress. Front Plant Sci 5:771. https://doi.org/10.3389/fpls.2014.00771

    Article  PubMed  PubMed Central  Google Scholar 

  70. Tolivia D, Tolivia J (1987) Fasga: a new polychromatic method for simultaneous and differential staining of plant tissue. J Microsc 148:113–117

    Article  Google Scholar 

  71. Verhertbruggen Y, Marcus SE, Knox JP (2013) Cell wall pectic arabinans influence the mechanical properties of Arabidopsis thaliana inflorescence stems and their response to mechanical stress. Plant Cell Physiol 54:1278–1288

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  72. Vianello A, Dell’Antone P, Macri F (1982) ATP- dependent and ionophore induced proton translocation in pea stem microsomal vesicles. Biochem Biophys Acta 689:89–96

    CAS  Article  Google Scholar 

  73. Whitney SCE, Gothard MGE, Mitchell JT, Gidley MJ (1999) Role of cellulose and xyloglucan in determining the mechanical properties of primary plant cell walls. Plant Physiol 83:272–277

    Google Scholar 

  74. Yruela I, Pueyo JJ, Alonso PJ, Picorel R (2005) Photoinhibition of photosystem II from higher plants: effect of copper inhibition. J Biol Chem 271:27408–27415

    Article  Google Scholar 

  75. Zamski E, Starkman F, Zieslin N (1991) Mechanical strength and anatomical structure of the peduncles of rose (Rosa x hybrida) flowers. Isr J Bot 40:1–6

    Google Scholar 

  76. Zhang Z, Zhang X, Wang S, Xin W, Tang J, Wang Q (2013) Effect of mechanical stress on cotton growth and development. PLoS ONE 8:e82256. https://doi.org/10.1371/journal.pone.0082256

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  77. Zeewart JA, Creelman RA (1988) Metabolism of abscisic acid. Annu Rev Plant Physiol Plant Mol Biol 39:439–473

    Article  Google Scholar 

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Acknowledgements

The authors are grateful to “Image UP” (Service de Microscopie et d'Imagerie Scientifique) at the University of Poitiers, for the precious technical help in Zeiss and TEM observations.

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FL, GR and RA conceived the experiments; PM, EB and PFL realized the experiments; PM, GR, EB, PFL and RA analysed the data; RA wrote the manuscript.

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Correspondence to Rossitza Atanassova.

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Michonneau, P., Roblin, G., Béré, E. et al. Adaptive responses of miniature rose to cultivation modes and abiotic stresses. Trees (2021). https://doi.org/10.1007/s00468-020-02079-3

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Keywords

  • Cultivation mode and abiotic stresses
  • Lignin content and monomer composition
  • Rose-bush architecture
  • Stem cyto-histology
  • Vascular sap nutrients